The ion transport properties of the mammalian descending colon have been the subject of numerous investigations during the last decade. In contrast, relatively few studies have investigated proximal segments of this organ. In the present study, we assessed transepithelial transport of Na+, K+ and Cl- in the isolated initial segment (P1) of rabbit colon in vitro using radioisotopic tracer fluxes and electrophysiological techniques. Like the rabbit descending colon, the proximal colon actively absorbs sodium and chloride, however, its transport systems are markedly different. In vivo, this segment absorbs potassium, however in vitro active potassium secretion was observed. Unlike the descending colon, Na+ absorption is relatively insensitive to amiloride and only a slight inhibition was obtained even at 1 mM concentrations of this drug. Na+ and Cl- absorption appeared to be coupled (directly or indirectly) since the absorption of each ion was inhibited by the removal of the other. Serosal ouabain also inhibited Na+ and Cl- absorption and net K+ secretion. Unlike the descending colon, the proximal P1 segment did not have a net absorptive K+ transport system that was detectable in the presence of ouabain. Electrically, the early proximal colon has a low transepithelial resistance compared to descending colon (RT = 133 +/- 7 omega cm2) but a larger short-circuit current (Isc = 178 +/- 12 microA/cm2). The transepithelial potential averaged -21 +/- 1 mV, in excellent agreement with values measured in vivo. The apical and basolateral membrane potentials averaged -21 +/- 1 mV and -42 +/- 1 mV and intracellular potassium activity was 70 +/- 2 mM.(ABSTRACT TRUNCATED AT 250 WORDS)